Diurnal changes in retinal nerve fiber layer thickness
with obstructive sleep apnea/hypopnea syndrome
Niphon
Chirapapaisan1, Techawit Likitgorn1, Mintra Pleumchitchom1,
Darin Sakiyalak1, Wish Banhiran2, Manatsawin Saiman1,
Wanicha Chuenkongkaew1
1Department of Ophthalmology, Faculty of
Medicine Siriraj Hospital, Bangkok 10700,
Thailand
2Department of Otorhinolaryngology, Faculty
of Medicine Siriraj Hospital, Bangkok 10700,
Thailand
Correspondence to: Niphon
Chirapapaisan. Department of
Ophthalmology, Faculty of
Medicine Siriraj Hospital, 2 Prannok, Bangkoknoi, Bangkok 10700, Thailand.
niphon.chi@mahidol.ac.th
Received: 2015-04-04
Accepted: 2015-11-04
Abstract
AIM: To
compare the retinal nerve fiber layer (RNFL) thickness in the morning and
evening in Thai patients with varying degrees of obstructive sleep
apnea/hypopnea syndrome (OSAHS).
METHODS:
In this
cross-sectional study, potential OSAHS patients at Siriraj Hospital underwent
polysomnography to determine the severity of OSAHS and an eye examination
(including best corrected visual acuity, slit-lamp examination, and Goldmann
applanation tonometry). RNFL thickness was recorded once in the morning and
once in the evening, using spectral domain optical coherence tomography. Thickness
was expressed as an average and given for each quadrant. Patients with ocular
or systemic diseases that might affect RNFL thickness were excluded.
RESULTS:
Forty-one
eyes of 41 patients were classified into 4 OSAHS groups. The average and mean
RNFL thickness in most of the four quadrants of the severe OSAHS group trended
toward being less than those in the comparable quadrants of the other groups in
both the morning and evening. In the moderate OSAHS group, the average RNFL
thickness and temporal and superior quadrant thickness in the morning were
significantly higher than in the evening (P=0.01, P=0.01, and P=0.03, respectively). In the severe
OSAHS group, the inferior quadrant thickness in the morning was significantly
higher than in the evening (P=0.03).
CONCLUSION:
The RNFL thickness in the morning was higher than in the evening in
moderate OSAHS.
KEYWORDS:
retinal nerve fiber layer thickness; sleep
apnea/hypopnea syndrome; optical
coherence tomography.
DOI:10.18240/ijo.2016.07.07
Citation: Chirapapaisan
N, Likitgorn T, Pleumchitchom M, Sakiyalak D, Banhiran W, Saiman M,
Chuenkongkaew W. Diurnal changes in retinal nerve fiber layer thickness with obstructive
sleep apnea/hypopnea syndrome. Int J Ophthalmol
2016;9(7):979-983
INTRODUCTION
Obstructive sleep apnea/hypopnea syndrome
(OSAHS) is characterized by repetitive episodes of upper airway occlusion
during sleep, associated with or without hypoxic changes in various tissues.
Severity of OSAHS is determined by total episodes of apnea (a pause in breathing)
and hypopnea (decrease in airflow during breathing with oxygen desaturation).
Average numbers of apnea episodes plus hypopnea episodes per hour of sleep
time, the apnea-hypopnea index (AHI), is used widely to classify OSAHS severity[1]. Studies[2-4] have shown OSAHS to be an independent
risk factor for the development of hypertension, cardiovascular morbidities,
cerebrovascular diseases, and poor quality of life from excessive daytime
somnolence. Additionally, several studies[2,5-11] have demonstrated an association between OSAHS and ophthalmic
conditions such as floppy eyelid syndrome, papilledema, optic neuropathies in
the form of nonarteritic anterior ischemic optic neuropathy (NAION), and
glaucoma. Correlations have been found between OSAHS and clinical features of
glaucoma such as retinal nerve fiber layer (RNFL) thinning, glaucomatous optic
disc changes, visual field defects, and increased intraocular pressure (IOP)[11-16]. Glaucoma causes RNFL thinning as early as
6y before visual field loss[17], thus determinations of RNFL thickness may
help in the early diagnosis and monitoring of this disease[18-19]. Furthermore, the relationship between OSAHS and RNFL thickness
may be dependent on OSAHS severity[11-13,16,20]. Optical coherence tomography (OCT) is noninvasive, noncontact, rapid, reliable and sensitive
to measuring small changes in RFNL thickness. Therefore, for clinicians, this
could provide a method to monitor OSAHS episodes and the OSAHS-associated
progression of eye damage. For patients, this could translate into better
control of apnea episodes, and methods to monitor treatment efficacy.
Although several mechanisms have been
proposed to explain optic neuropathies in OSAHS, the exact mechanism remains
unknown. Proposed theories include direct hypoxic injury to the optic nerve,
disrupted autoregulation of blood flow to the optic nerve from multiple periods
of hypoxia and hypercapnia, or disruption of blood flow during periods of
hypotension during sleep[11-12,15,21]. It is well known that ischemia results in tissue swelling in the
acute phase. Increased RNFL thickness was also found during the acute stage of
NAION, compared with the normal fellow eye[22]. Huseyinoglu et al[16] suggested optic nerve head changes start
with subtle optic disc edema in mild and moderate OSAHS patients, followed by
RNFL loss in cases of severe OSAHS. Whether the RNFL in OSAHS patients becomes
swollen after repetitive hypoxia during sleep is unknown. To our knowledge,
there is currently no existing report of diurnal RNFL changes in OSAHS patients
of more or less severity. In this study, we measured RNFL thicknesses of OSAHS
patients in the morning and in the evening. If hypoxic changes induced RNFL
swelling, the thickness in the morning would be higher than at other times of the
day and, possibly, this could contribute to further damage in more
severe OSAHS patients.
SUBJECTS AND METHODS
Study
Design and Subjects A cross-sectional study was conducted after approval from the
Siriraj Institutional Review Board. All subjects participated voluntarily and
gave their written informed consent.
We recruited 41 new subjects without any
prior OSAHS therapies, clinically suspected to have OSAHS as diagnosed by
snoring, observed pauses in breathing, and daytime sleepiness. To confirm OSAHS,
candidates were given a polysomnography test (PSG) at the Sleep Clinic,
Department of Otorhinolaryngology, Faculty of Medicine, Siriraj Hospital,
Mahidol University. Demographic data, including sex, age, height, body weight,
body mass index (BMI), and underlying systemic diseases were collected.
Ophthalmic
Examinations Each subject underwent a complete ophthalmic examination (8:00 a.m.) without knowing the results of the PSG.
Eye examination included best-corrected visual acuity (BCVA), automated refractometry,
Goldmann applanation tonometry, stereoscopic slit-lamp biomicroscopy, and
fundus examination. A 90-D lens was used to assess optic disc morphology and
retina background. The criteria used for subject inclusion were, 1) ≥18 years of age, 2) BCVA ≥20/40, and 3) spherical equivalent within ±5.0 D. Exclusion criteria were any ocular or
systemic diseases which might affect RNFL thickness, including diabetes
mellitus, glaucoma, age-related macular degeneration, and optic neuropathy.
RNFL thickness in each eye was measured by
OCT. This was performed by one trained ophthalmic technician using the spectral-domain OCT instrument (Heidelberg
Engineering, Heidelberg, Germany), which uses a tracking system to compensate
for eye movements. The details of the principles of spectral-domain OCT were previously described[23-24]. RNFL thickness was automatically segmented
using Spectralis v4.0. Minimum image quality was 15 dB. RNFL thickness was
measured twice for each patient. Evening (7:30 p.m.)
measurements were made on the same day prior to admission for overnight PSG.
Morning (8:00 a.m.) measurements were made the next morning
after discharge from the sleep laboratory. The measurements were obtained with
nondilated pupils. RNFL thicknesses were automatically generated for each of
four quadrants (superior, nasal, inferior, and temporal) and as an average
value. Both eyes of each subject were measured and recorded separately.
Sleep
Studies The standard overnight technician-attended PSG (Somte, Profusion
III software; Compumedics, Victoria, Australia) was performed on each patient.
Recordings included electroencephalograms, bilateral electrooculograms,
electromyograms, electrocardiograms, airflow measurements, respiratory
measurements, body position sensor recordings, and pulse oximetry measurements.
All PSG parameters were scored manually by well-trained sleep technologists,
and were reviewed by certified sleep specialists. Patients were then divided
into four groups according to their AHI: those without OSAHS (AHI<5), mild
OSAHS (5≤AHI<15), moderate OSAHS (15≤AHI<30), or severe OSAHS (AHI≥30).
Statistical
Analysis All data were analyzed using SPSS v11.5.0 (SPSS Inc., Chicago, IL,
USA). Demographic data are described as mean, range, and standard deviation for
continuous data and as numbers for categorical data. The left eye was selected
for analysis. Continuous data were compared among the groups using an
independent t-test and one-way analysis of variance (ANOVA) when
appropriate. Post-hoc analysis and Tukey’s multiple-comparisons test were used
for pairwise comparisons. Data within the same eye were compared using a
dependent t-test. Results were considered statistically significant at P≤0.05.
RESULTS
Forty-one eyes of 41 patients were
included in this study. Nine subjects (22%) did not have OSAHS (non OSAHS), 12
(29%) had mild OSAHS, 11 (27%) had moderate OSAHS, and 9 (22%) had severe OSAHS.
Demographic data are summarized in Table 1. The BCVA of each eye was 6/9 or
better (data not shown). No significant differences in age, BMI, and cup:disc
ratio were found among the four groups (P=0.92, 0.07, and 0.13, respectively, when compared with
control subjects). IOP was elevated but within the normal range in the severe
group only (P=0.04, one-way ANOVA);
this was not significant when compared with Tukey’s multiple comparison.
Table 1 Demographic information for each
OSAHS group
|
Parameters |
Non-OSAHS |
Mild OSAHS |
Moderate OSAHS |
Severe OSAHS |
1P |
|
No. of
eyes |
9 |
12 |
11 |
9 |
|
|
Male:Female |
2:7 |
7:5 |
7:4 |
7:2 |
|
|
Age
(a) |
49.4±9.1 |
53.1±8.2 |
50.5±18.2 |
51.3±11.9 |
0.92 |
|
BMI (kg/m²) |
24.5±6.3 |
26.5±3.7 |
29.8±4.9 |
28.5±3.3 |
0.07 |
|
AHI (h) |
2.2±1.5 |
12.0±7.9 |
20.2±3.6 |
64.4±25.5 |
|
|
IOP (mm Hg) |
14.2±1.6 |
14.3±2.7 |
14.3±2.3 |
16.5±4.2 |
0.04 |
|
C:D ratio |
0.28±0.03 |
0.34±0.06 |
0.33±0.06 |
0.34±0.05 |
0.13 |
OSAHS: Obstructive sleep apnea/hypopnea
syndrome; BMI: Body
mass index; AHI:
Apnea-hypopnea index; IOP:
Intraocular pressure; C:D ratio:
Cup:disc ratio; Non-OSAHS, AHI<5; Mild OSAHS, 5≤AHI<15; Moderate OSAHS,
15≤AHI<30; Severe OSAHS, AHI≥30. All data are presented as mean±standard
deviation. 1One-way
ANOVA.
The average RNFL and mean RNFL thickness
in most of the four quadrants of the severe OSAHS group trended toward being
less than those in the comparable quadrants of the other groups in both the
morning and evening. However, there were no statistically significant
differences. The mean RNFL thicknesses in each sector of all groups are shown
in Table 2.
Table
2 Mean
RNFL thickness in the morning and evening from each OSAHS group
|
RNFL sector |
Mean RNFL
thickness (µm) |
||||
|
Non-OSAHS |
Mild OSAHS |
Moderate OSAHS |
Severe OSAHS |
1P |
|
|
Morning |
|
|
|
|
|
|
Average |
105.11±9.55 |
102.08±12.35 |
108.27±13.37 |
99.66±5.54 |
0.33 |
|
Temporal |
85.00±14.32 |
89.00±19.03 |
87.09±17.76 |
74.44±13.15 |
0.23 |
|
Superior |
139.66±12.52 |
133.33±19.46 |
142.04±16.73 |
134.77±15.01 |
0.57 |
|
Nasal |
64.11±11.21 |
54.00±18.65 |
63.00±13.48 |
60.11±7.42 |
0.32 |
|
Inferior |
133.27±14.90 |
135.58±16.10 |
140.45±18.70 |
129.22±9.71 |
0.44 |
|
Evening |
|
|
|
|
|
|
Average |
104.44±8.03 |
102.00±12.44 |
107.00±13.28 |
99.66±5.40 |
0.46 |
|
Temporal |
84.77±13.55 |
89.16±18.20 |
86.18±17.26 |
75.33±14.38 |
0.28 |
|
Superior |
139.27±10.68 |
132.95±19.67 |
139.81±17.24 |
135.27±15.01 |
0.72 |
|
Nasal |
61.66±7.41 |
53.83±18.32 |
62.54±12.93 |
59.33±7.51 |
0.39 |
|
Inferior |
131.88±12.62 |
136.12±17.93 |
139.09±17.66 |
127.88±10.16 |
0.40 |
RNFL:
Retinal nerve fiber layer; OSAHS:
Obstructive sleep apnea/hypopnea syndrome; Morning: 8:00 a.m.; Evening: 7:30 p.m.
Results are presented as mean±standard deviation. Groupings are based on the
apnea-hypopnea indices as described in Table 1. 1One-way
ANOVA with significance at <0.05.
Differences in RNFL thickness measured in
the morning and evening are shown in Table 3. In the moderate OSAHS group, the
RNFL was significantly thicker in the morning than in the evening as an average
value and in the temporal and superior quadrants (P=0.01, 95%CI 0.36-2.17; P=0.01, 95%CI 0.20-1.61; and P=0.03,
95%CI 0.26-4.19, respectively), but not in the other quadrants. In the severe
OSAHS group, diurnal differences in RNFL thicknesses were found only in the
inferior quadrant (P=0.03, 95%CI 0.08-2.57).
Table
3 Diurnal
differences and 95%CI of the mean RNFL thickness in each of four sectors
between morning and evening and the average for the four categories of patients
with OSAHS
|
Groups |
RNFL
sector |
Mean
RNFL thickness (µm) |
1P |
|
|
Difference |
95%CI |
|||
|
Non-OSAHS |
Average |
0.66 |
-1.4,
2.73 |
0.47 |
|
|
Temporal |
0.22 |
-1.39,
1.84 |
0.76 |
|
Superior |
0.38 |
-2.29,
3.07 |
0.74 |
|
|
Nasal |
2.44 |
-1.67,
6.56 |
0.20 |
|
|
Inferior |
1.38 |
-1.95,
4.72 |
0.36 |
|
|
Mild OSAHS |
Average |
0.08 |
-0.34,
0.5 |
0.67 |
|
|
Temporal |
-0.16 |
-0.87,
0.54 |
0.61 |
|
Superior |
0.37 |
-0.21,
0.96 |
0.19 |
|
|
Nasal |
0.16 |
-0.36,
0.69 |
0.5 |
|
|
Inferior |
-0.54 |
-2.04,
0.95 |
0.44 |
|
|
Moderate OSAHS |
Average |
1.27 |
0.36,
2.17 |
0.01 |
|
|
Temporal |
0.90 |
0.20,
1.61 |
0.01 |
|
Superior |
2.22 |
0.26,
4.19 |
0.03 |
|
|
Nasal |
0.45 |
-0.36,
1.27 |
0.24 |
|
|
Inferior |
1.36 |
-0.6,
3.33 |
0.15 |
|
|
Severe OSAHS |
Average |
0 |
-0.54,
0.54 |
1 |
|
|
Temporal |
-0.88 |
-2.75,
0.97 |
0.3 |
|
Superior |
-0.50 |
-2.14,
1.14 |
0.5 |
|
|
Nasal |
0.77 |
-0.29,
1.85 |
0.13 |
|
|
Inferior |
1.33 |
0.08,
2.57 |
0.03 |
|
RNFL: Retinal nerve fiber layer; OSAHS:
Obstructive sleep apnea/hypopnea syndrome; CI: Confidence interval. Groupings are
based on the apnea-hypopnea indices as described in Table 1. Statistical
significance was set at <0.05. Difference: the difference in thickness between
morning (8:00 a.m.) and
evening (7:30 p.m.) as
measured by optical coherence tomography and expressed in microns. 1By
independent t-test.
Thirty-three
(80.4%) subjects slept in the supine position most of the time and the episodes
of apnea and hypopnea. Four (9.8%) and 4 (9.8%) subjects slept on their right
or left side. No subjects slept in the prone position. There was no
relationship between sleep position and RNFL thickness.
DISCUSSION
We found RNFL thicknesses to be lower in
the severe OSAHS group. This was consistent with results from previous studies[11-13,20]. As
proposed in previous studies, thinning of RNFL in severe OSAHS individuals may
result from partial axonal death, which is a consequence of chronic hypoxia[11-14]. However, in the present study the lower
RNFL thickness was not statistically significant. This may have been because of
our small sample size as well as differences in disease onset.
In the present study, we determined if
spectral domain OCT was useful to assess diurnal variations in RNFL thicknesses
of patients with varying severity of OSAHS. RNFL thickness in patients with no
and mild OSAHS did not differ between morning and evening, but those with
moderate and severe OSAHS showed some significant differences (Table 3). During
sleep, repetitive upper airway obstructions in OSAHS could cause insufficient
optic nerve head blood flow and hypoxia[11-14].
This may induce optic nerve ischemia and subsequent RNFL swelling, eventually
leading to cell death. Consequently, measurements of RNFL thickness in the
early morning may be higher than at other times of the day, depending on the
severity of the OSAHS. However, the RNFL thickness changes in the morning were
small, and not clinically significant. The OCT could be a method to monitor
visual disease in OSAHS and clinicians would not need to consider the time of
day when measuring RNFL.
Swelling of RNFL might also occur in
papilledema, from increasing cerebral spinal fluid (CSF) pressure during sleep,
due to chronic hypercapnia, induced vasodilatation, and increased cerebral
blood volume[8-9,25]. A previous study reported OSAHS patients
with symptoms of idiopathic intracranial hypertension but no sign of a disc
edema[25], which could have been from subclinical
papilledema. This would not be detected by a fundus examination but could be
apparent as a swelling of RNFL in OCT images. During the day, with no
upper airway obstruction, optic nerve perfusion would be improved, CSF pressure
would not be elevated, and RNFL may not become swollen.
RNFL thickness in the severe OSAHS group
was thinner than that in moderate OSAHS. Detection of RNFL swelling in thinner
RNFL thickness may be more difficult because of the thinness of the layer and
the lower level of hypoxia required to induce substantial swelling. This may
indicate induced partial axonal death due to chronic hypoxia and RNFL loss in
the severe OSAHS group. A thin RNFL with partial axonal death in patients with
severe OSAHS may not show significant RNFL swelling; thus, a change in RNFL
thickness secondary to acute hypoxia may not be observed in some quadrants of
the eyes in such patients. These findings support our hypothesis that
significant hypoxic changes during OSAHS may result in RNFL swelling, and ultimately
as the disease progresses, in RNFL loss from chronic intermittent hypoxia or
ischemia.
During
sleep, chronic intermittent upper airway obstructions in OSAHS resulted in
insufficient optic nerve head blood flow, direct hypoxic damage to the optic
nerve and progressive thinning of RNFL and choroidal thickness[11-13,20-21]. Subclinical RNFL thinning caused from
OSAHS can be detected by OCT, but may be misdiagnosed as glaucoma. In this
case, the appropriate treatment to prevent RNFL loss should be OSAHS management,
not drugs which lower IOP.
IOP
and fluctuation of IOP play a role in glaucomatous optic nerve head damage[26]. The trans-lamina cribrosa pressure (TLCP)
difference is the most important factor in the physiology and pathophysiology
of the optic nerve[27-29]. The
TLCP difference depends on the retrobulbar CSF pressure and IOP[30]. Thus, TLCP fluctuations depend on either
the CSF pressure or IOP fluctuation. In patients with OSAHS, fluctuations in
the CSF pressure during the day and night cause fluctuations in the TLCP and
might be a factor in optic nerve head damage.
In
the severe OSAHS group, RNFL thickness was less than in the other groups;
however, the BCVA in all eyes was 6/9 or better. This suggests that decreases
in RNFL thickness do not immediately result in decreased visual acuity.
However, a previous study reported that multifocal visual evoked potentials
detected early subclinical optic nerve abnormalities in patients with OSAHS[31].
There
are limitations to the present study. Unfortunately, we did not collect data on
other visual functions, and the sample size was relatively small. The time
varied from onset of symptoms to disease diagnosis and examination, and longer
durations of OSAHS may have affected RNFL thinning from chronic hypoxia. Finally,
although OCT is less invasive and provides a quantitative measurement of RNFL
thickness, spectral domain OCT may not be sensitive enough to detect diurnal
acute changes in RNFL and does not provide any functional visual information.
Cohort studies of RNFL thickness and visual function analyses, such as visual
field or contrast sensitivity measurements, may provide more information on how
OSAHS induces abnormalities of RNFL.
In
conclusion, impaired optic nerve head perfusion and hypoxia from repetitive
upper airway obstructions in OSAHS may initially induce optic nerve ischemia
and RNFL swelling. In general, RNFL thickness measurements taken in the morning
can be expected to be above the diurnal average in OSAHS patients, and these
measurements could vary with the severity of the OSAHS. Chronic intermittent
hypoxia could induce partial RNFL death and loss in patients with severe OSAHS,
and this could be determined using OCT.
ACKNOWLEDGEMENTS
Some
parts of this study were presented at the 11th European Neuro-Ophthalmology
Society Meeting.
The
authors thank Dr. William Beamish for reviewing the manuscript.
Foundation: Supported partially by the Siriraj Hospital Research
Fund, which helped to develop ophthalmology research. The funding organization
had no role in the design or conduct of the research.
Conflicts
of Interest: Chirapapaisan N, None; Likitgorn T, None; Pleumchitchom M, None;
Sakiyalak D, None; Banhiran W, None; Saiman M, None; Chuenkongkaew
W, None.
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